Gayle started his career at Brentford in 1988, scoring 26 goals in 193 appearances for the Bees. He was loaned to KuPS in 1990, before becoming a regular player in the Brentford side under new manager Phil Holder in 1990–91, when the Bees qualified for the playoffs but lost to eventual promotion winners Tranmere Rovers in the semi finals. He played 33 games in the Third Division that season, scoring six goals. He was a key part in their Third Division title success for the 1991–92 season, scoring 6 goals in 38 games to give Brentford a place in the new Division One, as the old Second Division would be known from the start of the 1992–93 campaign due to the creation of the FA Premier League. The 1992–93 season looked as though it would be a successful one for the Bees, who entered the new year in 10th place and on the brink of the playoff zone, with all the talk at Griffin Park being about a second successive promotion and top division football for the first time since 1947. However, a collapse in the second half of the season saw the Bees relegated. Gayle initially remained loyal to the Bees, but on 24 March 1994 he linked up with his old Brentford striker partner Gary Blissett in a £250,000 move to Wimbledon, who were in the process of finishing a creditable sixth place in the Premier League.

Gayle played an influential part during the nineties, He made his debut for Wimbledon two days after joining them as they beat Leeds United 1–0. He played in their final 10 games of the 1993–94,helping the dons to 7 wins 2 draws but unfortunately did not score. He scored his first two goals in 1994–95, playing 23 games as the Dons finished ninth. He missed just four league games in the 1995–96 season, scoring five goals and helping Wimbledon finish 14th. In his best season for the Dons, 1996–97, he scored a total of thirteen goals, eight league goals as the Dons finished eighth in the Premier League and reached the semi finals of both domestic cups. He also scored the winning goal for the Dons in a surprise FA Cup fourth round replay 1–0 win over Manchester United in February 1997.[2]

1997–98 was less successful. The Dons began the season well and were in the top five for much of the first half of the season, but a dismal second half of the campaign saw them finish 15th. Gayle was a regular player once again, appearing 30 times in the league, but scored just twice.Gayle's form was good enough to make his debut for Jamaica in February vs the mighty Brazil in the gold cup and later featuring in the 1998 world cup in France that summer. He was their top scorer in 1998–99, scoring 10 league goals, but once again their good form tailed away to a late season slump and they finished 16th. He did manage seven goals in 1999–2000, but defeat to Southampton on the final day of the season and a surprise win for relegation rivals Bradford City over Liverpool meant that Wimbledon's 14-year stay in the top flight was over. In seven years with the Dons, Gayle played 285 games scoring 48 goals .

Gayle initially stayed loyal to the Dons in spite of their relegation, playing 32 league games and scoring three times in the 2000–01 campaign before he finally departed on 9 March 2001 in a £1million move to Scottish Premier League giants Rangers. He made his debut against Dundee United, adding just another three more appearances, before moving back down south to join Gianluca Vialli's new look Watford side for £1million.[3]

He played just four times for the Gers until a close season return to England when he joined Watford for £900,000. He started off brightly by scoring five goals in first 14 matches until a back injury hampered his season . he was as expected to leave, along with most of Vialli's other unsuccessful signings, in the summer of 2002. However, he re-emerged as a centre-back under new manager Ray Lewington, and won the Player of the Season award that year. He also scored in the club's 2–1 defeat to Southampton in the FA Cup semi-finals and part of the group of players that deferred some of their wages to help the club out of their financial difficulties .Another good season followed in 2003–04 forging a good partnership alongside captain Neil cox, but injury plagued his 2004–05, and he left Watford two days after the sacking of Lewington in March 2005.

He re-joined Brentford, his first club and made 37 appearances for the Bees helping them to two consecutive play off semi finals, scoring twice. Gayle was released from his Brentford contract on 17 May 2006.

He signed for Aldershot Town on 2 July 2006. He scored the first hat-trick of his career for the Shots on 14 October 2006, coming on as a second-half substitute to score three times in just 9 mins 30 seconds against Kidderminster Harriers.[4] In February 2007 Gayle damaged his ACL knee ligaments and cartilage, but still made the last few matches of the season he was released by Aldershot at the end of 2006–07 season scoring seven times in 28 appearances.

He was signed for AFC Wimbledon in May 2007 by former Aldershot manager Terry Brown, making him only the second player to play competitively for both AFC Wimbledon and the old Wimbledon FC (the first being Jermaine Darlington)[5] and, after scoring against Maidenhead United in the FA Trophy,[6] becoming the only player to have scored for both incarnations of the South West London club and helping them to promotion to the conference south before retiring from playing that summer.

Gayle was capped by England at U17 level but later decided to switch allegiance and play for Jamaica who he was eligible to represent through his father. When a player at Wimbledon, Gayle signed a contract in June 1997 with a clause that restricted him to only represent England at international level. Horace Reid of the Jamaica Football Federation complained to FIFA about the restriction and the FIFA Player Status Committee refused to recognise the clause and allowed Gayle to change allegiance to Jamaica in January 1998.[7]

Gayle was capped 14 times for Jamaica and played at the 1998 CONCACAF Gold Cup in United States and the 1998 FIFA World Cup in France.Jamaica's first ever World Cup finals .Gayle didn't play in the 3–1 defeat by Croatia at the Stade Félix-Bollaert, 13] Or as Jamaica lost 5–0 to Argentina at Parc des Princes, but did play in the final group H match and beating Japan 2–1 at Stade de Gerland.[14][15]. Gayle was made captain the following year vs Canada and held that honour for a year before retiring.

He announced his retirement from competitive football after AFC Wimbledon sealed promotion to the Conference South following a 2–1 Isthmian League Premier play-off final victory over Staines Town.[8][9] He is presently working towards his coaching badges and in September 2008 took the role of AFC Wimbledon reserve team manager. In his first year of taking over he guided his talented squad to two cup finals, winning the suburban league challenge cup and runners up in the suburban challenge shield in 2009. Runners up in the league came in 2010. In 2011, his reserves collected the league trophy for the very first time and also the champions cup, very unlucky not to pick up the treble after losing to South Park in the Suburban Premier Cup.[10] Marcus is a member of the Wimbledon Old Players Association and has played for Wimbledon's Masters side and Old Players XI.[9]

On 15 May 2012, it was announced that Marcus had been appointed as first team manager of Staines Town.